| dc.description.abstracteng | The pulvinar is the largest thalamic structure in the center of the brain, reciprocally connected to a large diversity of cortical areas. It has grown more than other subcortical structures during primate evolution, which is one of the reasons why it is thought to be crucial to primate behavior. Taking the few studies on pulvinar electrophysiology and perturbation together, it is clear that the function of pulvinar is complex, and might be involved in a wide range of cognitive processes such as allocation of spatial attention, target selection, motor coordination, and even emotional processing or confidence. What most of the recent studies agree upon is that its function is strongly linked to voluntary movements, going well beyond purely relaying sensory information to cortical areas as initially thought, and making pulvinar a particularly interesting target for understanding the neuronal substrates of goal-directed behavior in primates. Especially the non-retinotopically organized, dorsal aspect of the pulvinar remains understudied and its contribution to perceptual and motor intentional processing remains speculative. Further investigation of dorsal pulvinar function in these processes should contribute to our understanding of how the brain processes visual information in order to select and execute appropriate actions and help to elucidate the function of this mysterious structure which has puzzled researchers for the last decades. Here, we provide new evidence of dorsal pulvinar involvement in goal-directed behavior, contributing to the ongoing discussion in the field about the role of pulvinar in visuomotor processing using a battery of different approaches in behaving macaque monkeys and humans.
First, we analyzed visual and motor related neuronal processing in the dorsal pulvinar during basic oculomotor tasks, visually-guided and delayed memory-guided saccades. In the memory-guided task, visual responses were more pronounced, time-locked and space specific (predominately contralateral), but overall pulvinar exhibits more motor related activity, in some cells prior to and during saccades, but mostly in the post-saccadic period. The patterns of motor-related activity were diverse, spanning contralateral and ipsilateral spatial tuning and also motor-related enhancement and suppression. Despite strong connectivity to parietal cortex, in this task most pulvinar cells did not show classical visuomotor delay period activity or pre-saccadic ramping of firing. Instead, delay period activity was typically suppressed (relative to initial fixation period) with no spatial preference, and delay period activity did not predict the upcoming movement in free-choice trials when two saccade options were available. However, on the level of synaptic processing represented by the local field potentials, the upcoming choice was encoded, suggesting that in principle the information about target selection was present before motor execution. Moreover, we show that a subset of pulvinar neurons exhibits properties similar to gain fields related to gaze position, suggesting that pulvinar encodes space not only in eye-centered, retinotopic reference frame, and might also be involved in visuomotor transformations.
To further assess the role of pulvinar function in target selection we investigated effects of dorsal and ventral pulvinar microstimulation in similar oculomotor tasks. Systematic variation of stimulation times relative to the behavioral states and stimulus/saccade onset revealed space-specific, time-specific, task-specific, and site-specific involvement of pulvinar in target selection, evident in microstimulation-induced modulation of spatial decisions in free-choice trials, and effects on saccadic reaction times. These results suggest that the dorsal pulvinar influences target selection when the decision and action are in close temporal proximity, and not when the visual processing and the motor response are separated by the intervening memory delay period.
One of main outstanding questions in studying spatial choice processing in general and in pulvinar research in particular is whether behavioral effects of causal perturbations or neurological lesions stem from perception or motor intention impairments. To dissociate sensory-perceptual and motor-intentional aspects of spatial deficits, we designed a novel “search-to-sample” task and tested in in groups of young and elderly human subjects and in the macaque monkey. The comparative aspect of this work was intended to establish experimental approaches that would allow drawing parallels between studies in neglect patients and in reversible pharmacological inactivation-based macaque model of spatial deficits. Although the effects of MRI-guided pulvinar inactivation in this task were small, they further support the idea that pulvinar is involved in motor-intentional processing, especially when compared with effects after control inactivation of the cortical temporal parietal occipital area (TPO) in the same monkey. The electrophysiological characterization of the area TPO however suggested considerable similarities between encoding of visuospatial and motor contingencies between this area and the dorsal pulvinar. Given that these two regions are both anatomically and functionally connected, this shows that functional contribution of specific regions has to be considered not in isolation but within the interconnected circuitry. At the same time, these data emphasize the importance of combining “correlative” recordings with causal interference approaches.
Additionally, we tested saccadic, grasping and reaching deficits of a patient with rare bilateral pulvinar lesion. The patient exhibited mainly postural deficits, specifically when reaching with the right hand (contralateral to the more pronounced lesion), accompanied by general slowing of movements and grasping deficits. These findings further support the idea that pulvinar might be involved both in guiding goal-directed actions and more specifically in sensorimotor transformations. In combination with findings from other related projects in our group, the results of this thesis indicate that the function of the dorsal pulvinar goes well beyond purely visuospatial or attentional processing. | de |